Abstract
BackgroundFor the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized. One way to achieve this is local remodeling of the circuitry hardwiring. To genetically investigate the underlying mechanisms of this remodeling, one model system employs a major group of Drosophila multidendritic sensory neurons - the dendritic arborization (da) neurons - which exhibit dramatic dendritic pruning and subsequent growth during metamorphosis. The 15 da neurons are identified in each larval abdominal hemisegment and are classified into four categories - classes I to IV - in order of increasing size of their receptive fields and/or arbor complexity at the mature larval stage. Our knowledge regarding the anatomy and developmental basis of adult da neurons is still fragmentary.ResultsWe identified multidendritic neurons in the adult Drosophila abdomen, visualized the dendritic arbors of the individual neurons, and traced the origins of those cells back to the larval stage. There were six da neurons in abdominal hemisegment 3 or 4 (A3/4) of the pharate adult and the adult just after eclosion, five of which were persistent larval da neurons. We quantitatively analyzed dendritic arbors of three of the six adult neurons and examined expression in the pharate adult of key transcription factors that result in the larval class-selective dendritic morphologies. The 'baseline design' of A3/4 in the adult was further modified in a segment-dependent and age-dependent manner. One of our notable findings is that a larval class I neuron, ddaE, completed dendritic remodeling in A2 to A4 and then underwent caspase-dependent cell death within 1 week after eclosion, while homologous neurons in A5 and in more posterior segments degenerated at pupal stages. Another finding is that the dendritic arbor of a class IV neuron, v'ada, was immediately reshaped during post-eclosion growth. It exhibited prominent radial-to-lattice transformation in 1-day-old adults, and the resultant lattice-shaped arbor persisted throughout adult life.ConclusionOur study provides the basis on which we can investigate the genetic programs controlling dendritic remodeling and programmed cell death of adult neurons, and the life-long maintenance of dendritic arbors.
Highlights
For the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized
This reorganization of initial neural circuits formed during early development is critical to support a wide range of animal behaviors under a variety of environmental contexts [1,2]
We found that markers for subsets of larval da neurons were not necessarily reliable tracers to pursue the relationship between larval da neurons and the pharate adult da cells
Summary
For the establishment of functional neural circuits that support a wide range of animal behaviors, initial circuits formed in early development have to be reorganized. The nervous system is reorganized at multiple structural levels to strengthen, elaborate, and/or modify already acquired functions, and even add novel ones This reorganization of initial neural circuits formed during early development is critical to support a wide range of animal behaviors under a variety of environmental contexts [1,2]. One cellular mechanism of this reorganization is the disposal of a subset of early-born neurons and replacement of those cells with later-born ones Another is 'recycling,' which is accomplished by pruning of axons or dendrites without loss of parental neurons and concomitant or subsequent growth of these processes in spatially distinct patterns [35]. Remodeling of stage-specific dendritic patterns is an essential process to realize the proper function of the nervous system
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